Japanese Society of Grassland Science ISSN1744-6961

SHORTBlackwellMeGRSGr1744-6961©XXXCaseHaR. 2008Ishiwakaasslandrvlbourne, estReports Blackwell mouse PublishingScience andAustralia as Y. Publishing aMasuda control Asia agent Ltd REPORT Possible biological control of the armyworm by the harvest mouse Reiko Ishiwaka and Yasuhisa Masuda

Laboratory of Feed Science, Faculty of Agriculture, Kyushu University, Fukuoka, Japan

Keywords: Micromys minutus, separate, pest control. Received: 22 February 2007; accepted 09 October 2007 Correspondence: Reiko Ishiwaka, Laboratory of Animal Feed Science, Faculty of Agriculture, Kyushu University, 6-10-1 Hakozaki, Higashi-ku, Fukuoka 812-8581, Japan. Email: [email protected] doi: 10.1111/j.1744-697X.2007.00105.x

and , specifically between a latitude of 45°N to 45°S, Introduction and a longitude of 60°E to beyond 170°W (Sharma & Davies The harvest mouse, Micromys minutus Pallas (Rodentia: 1983, cited by Sharma et al. 2002). Larvae of the armyworm Muridae), is highly adept at climbing grass leaves and stems feed on primarily leaves of gramineous plants and periodically with its remarkably small body size (7–9 g in adults), grasping causes serious damage to the following crops: sorghum hands and feet and a prehensile tail; this fact reveals how ( [L.] Moench), pearl millet (Pennisetum glaucum effectively this species has adapted to inhabit the stalk zone of [L.] R.Br.), O. sativa, (Zea mays L.), wheat (Triticum aestivum Gramineae communities (Ishiwaka & Mõri 1999). The harvest L.) and sugarcane (Saccharum officinarum L.) (Sharma et al. 2002). mouse is widely distributed in the temperate and humid This pest affects the following forage plants as well: perennial climate zone between East Asia and West Europe (Harris & ryegrass (Lolium perenne L.), orchardgrass (Dactylis glomerata Trout 1991). In most of the regions in this zone, Gramineae L.), reed canarygrass (Phalaris arundinacea L.), redtop (Agrostis communities progress to climax vegetation in which trees alba L.), and weeping lovegrass (Eragrostis curvula Nees) are dominant, unless disturbances such as burning, floods, (Watanabe 1961; Koyama & Watanabe 1962; Kanda et al. 1977). grazing or harvesting occur. Despite such a wide distribution, Yield losses are influenced largely by the stage at which the the International Union for Conservation of Nature (IUCN) damage occurs and the gregarious behavior of the larvae. has listed this species in the “near threatened” category since Sometimes, an outbreak results in complete crop loss. Out- 1996 (IUCN 2007). breaks of the armyworm in crop fields have been recorded The harvest mouse appears to be strongly associated with many times in South Asia (Lin et al. 1964; Thakur et al. 1987; agricultural lands including their surrounding grass strips Sharma et al. 2002). In Japan, serious damages to rice and other that are exposed to various disturbances (Harris & Trout 1991; gramineous crops have been reported frequently (Ohmori Bence et al. 2003; Moore et al. 2003; Surmacki et al. 2005). 1960; Koyama 1963, 1966, 1970; Oku & Kobayashi 1974; Oku Furthermore, in Japan, many harvest mice appear to inhabit et al. 1979; Hirai et al. 1985); in contrast, only sporadic outbreaks some gramineous crop fields and their edges (i.e. grass strips); have occurred in agricultural grasslands such as meadows this has occurred following the conversion of many river banks (Oku et al. 1976; Kanda et al. 1977; Kanda 1988). into concrete walls. The unique spherical nests of the harvest The use of insecticides has depressed the populations of mouse are often observed in rice ( L.) communities herbivorous to some extent, but their use is severely in paddy fields and in Imperata cylindrica (L.) Beauv. var. restricted, particularly in organic agriculture and forage crop koenigii (Retz.) Durand et Schinz communities in paddy levees. fields. Therefore, the biocontrol of pest insects has been inves- However, rice farmers sometimes remove these nests to prevent tigated in crop fields. Insectivorous birds, parasitic wasps as well damage to their crops. Compared with rice fields, the less inten- as predators such as spiders, and pathogens have sive management of agricultural grasslands such as meadows been studied in relation to the biocontrol of pest insects (e.g. and pastures allows the harvest mouse to maintain its popu- Fowler et al. 1991; Bock et al. 1992; Donovan 2003; Hooks lation, even though machinery, chemical fertilizer and intro- et al. 2003; Rosa and Simões 2004; Jones et al. 2005). duced crop plants are applied there (Tsukada et al. 2004; Forty-two parasitoids, 15 predators, four bacteria, five R. Ishiwaka, unpubl. data). fungi, and three viral strains have been reported as natural The armyworm, Walker (: control agents for the armyworm (Sharma & Davies 1983, ), is a pest of several cereal and forage crops in Asia cited by Sharma et al. 2002). The armyworm larvae tend to

52 Grassland Science 54 (2008) 52–56 © 2008 Blackwell Publishing Ltd R. Ishiwaka and Y. Masuda Harvest mouse as a control agent remain hidden under the ground or in the sheath of the host three cages, with one pair in every cage as treated condition, plant during the day, and they feed at night (Kanda 1988). It prior to release of the armyworm. Eighteen days after the is natural that the control agents for the armyworm should placing of the harvest mouse, we examined the guineagrass exclude bird species because most insectivorous ones are leaves in the cages with the harvest mouse to evaluate whether diurnal. Mammal species, on the other hand, usually become it can be a pest of this crop. The armyworm larvae in various more active at night; therefore, they can potentially depress instars were obtained from an infested sudangrass (Sorghum the populations of such nocturnal pest insects. However, to sudanense Piper [Stapf ]) crop field located 4 km east. Thirty-eight the best of our knowledge, studies on any omnivorous or to 40 individuals of the armyworm were placed inside each insectivorous mammal as a natural control agent for pest cage; they were transferred with similar instar composition to insects have not been available to date, except for a study by all the six cages on 1 November (19–21 individuals cage–1), Ellis et al. (2005), probably because mammal species, especially 3 November (4 individuals cage–1) and 19 November (15 rodents, have been generally regarded as little more than pests. individuals cage–1). In the armyworm, third instars can become Grassland scientists have generally discussed wildlife, especially pupae and no longer feed on leaves no earlier than 18 days at wild mammal species, primarily as pests or in relation to 20°C (Okuyama & Tomioka 1963). Therefore, the guineagrass biodiversity. We assumed that some omnivorous and insec- communities would be exposed to infestation by the army- tivorous mammal species including the harvest mouse would worm larvae at all times during the experiment. Water and food have the potential to modify the interaction between grami- were available for the harvest mouse ad libitum; the diet con- neous forage plants and pest insects as well as other control sisted of commercial laboratory mouse chow NMF (Oriental agents in agricultural grasslands. If function of such a mammal Yeast, Tokyo, Japan) along with the following seeds: canary as an extra biocontrol agent for pest insects is suggested, the grass, Chinese, foxtail, common millet, flax, and sunflower. establishment of integrated pest management in grasslands will be promoted. Moreover, with this study, conservation of a threat- Categorization of guineagrass leaves ened species can directly link to agricultural profitability. The aim of this study is to evaluate the effects of the harvest Forty days after placing the first armyworm larvae into the mouse on a gramineous forage plant infested by the army- cages, we sampled approximately 100 guineagrass leaves from worm. Because of the difficulty in establishment of authentic each cage at random. Then, we classified each of the leaves grassland from which only the harvest mouse is completely into one of five categories based on the infestation stage; removed, we adopted cages, in which the harvest mouse, the namely, the extent of consumption by the armyworm in armyworm and a forage grass were brought, on a crop field. terms of leaf area. The categories were as follows: intact leaves (no consumption detected); up to 25% of the leaf area consumed; between 25% and 50% of the leaf area consumed; Materials and methods between 50% and 75% of the leaf area consumed; and more than 75% of the leaf area consumed. The tendency of the Experimental condition armyworm to neglect midribs when feeding on grass leaves We used harvest mice from a colony established with five wild enabled us to estimate the damage it caused to the leaves in individuals captured in Saga, Kyushu, Japan in 1990. In May terms of dry weight. Based on the length of the midrib of a 2001, we built six cages sized 90 cm × 90 cm × 100 cm on the damaged leaf, we estimated the dry weight of the leaf before ground at a crop field in Fukuoka, Kyushu, Japan (5 m a.s.l.). consumption; this was done by means of a relationship curve The cages were made of wire mesh (5 mm × 5 mm) and wood. of the midrib length versus the dry weight of more than 500 Guineagrass (Panicum maximum Jacq.), a kind of tropical intact leaves. The actual dry weight of the damaged leaves forage grass, was seeded inside and outside the cages. The top subtracted from the estimated dry weight before damage is of each cage was covered with a sheet of transparent vinyl equivalent to the yield loss caused by the armyworm. chloride in order to keep the harvest mouse from dying and its artificial food (described later) from decay. Every sheet Statistical analyses had holes through which rainwater fell in and all the guineagrass vegetations inside the cages were watered when needed, though We used a χ2 analysis for comparison between the frequency neither fertilized nor harvested. We had transplanted some distributions of the extent of leaf consumption by the individuals from the outside at a low density to establish similar armyworm. We replaced each category of intact to more than vegetations among the cages when the grass was still short. 75% with 0–4 as scores, respectively, and calculated a mean The cages were then left alone until the end of the experimental score of each cage. After Bartlett’s test for homogeneity of period. variances of the mean scores, a two-tailed Student’s t-test was On 13 October, when each cage was found to have a closed used for comparison between the presence and the absence of dense grass canopy, we placed six adult harvest mice into the harvest mouse. We again adopted a Student’s t-test for

Grassland Science 54 (2008) 52–56 © 2008 Blackwell Publishing Ltd 53 Harvest mouse as a control agent R. Ishiwaka and Y. Masuda comparison between the estimated yield losses in the presence which was significantly less than the figure of 7.47 ± 0.77 g and the absence of the mouse. from the cages without the mouse (P = 0.036).

Results Discussion No feeding sign of the harvest mouse was detected on The harvest mouse significantly reduced the damage of leaves guineagrass leaves. The frequency distribution of the extent by the armyworm, leading to a greater proportion of intact of leaf consumption by the armyworm is shown in Figure 1. leaves (i.e. lower proportion of damaged leaves), and resulted The frequency distributions of the extent of leaf consumption in a significant lowering of the estimated yield loss caused by by the armyworm were significantly different between the the armyworm. The results suggest that the harvest mouse presence and absence of the harvest mouse (χ2 analysis, has the potential to modify the interaction between gramineous P < 0.0001). The mean proportion of the intact leaves from forage plants and the armyworm through lessening the density the cages in which the harvest mouse was present (59.1 ± 2.1%, of the armyworm. The harvest mouse can live temporarily at mean ± standard error of the mean [SEM]) was greater than the density in this study, as some different individuals had that in the cages in which the harvest mouse was absent been caught at one trap station during a few consecutive days (35.0 ± 2.4%). Conversely, the mean proportion of those in (R. Ishiwaka, unpubl. data). The density of the armyworm in which the damage was between 50% and 75% of the leaf area this study has been often observed in the time of outbreaks. and the mean proportion of the leaves in which the damage Compared to gramineous crop fields under more intensive was more than 75% of the leaf area was lower in the cages with management, much fewer reports on outbreaks of the armyworm the mouse (5.7 ± 0.7% and 4.9 ± 1.6%, respectively) than those in agricultural grasslands have been published, in spite of the in the cages without it (10.4 ± 0.9% and 13.2 ± 1.1%, respectively). fact that gramineous plants are present in both. Structurally The mean proportion of the leaves in which the damage was complex landscapes with substantial areas of woody habitats up to 25% of the leaf area and the mean proportion of those and a limited agricultural area hold the potential for sustainable in which the damage was between 25% and 50% of the leaf pest control by natural enemies (Bianch et al. 2005), and agricu- area increased from 21.0 ± 3.6% and 9.2 ± 1.0% in the presence ltural intensification can have wide impacts on biodiversity of the harvest mouse, respectively, to 27.1 ± 1.8% and (Robinson & Sutherland 2002). The less the intensification 14.2 ± 2.2% in its absence, respectively. and the more complex the landscapes, and thus the more The mean score of infestation stages in the presence of the efficient the management of the habitat of some wildlife harvest mouse (0.76 ± 0.05, mean ± SEM) was significantly including the harvest mouse, may be associated with fewer lower than that in the absence (1.40 ± 0.09; Student’s t-test, outbreaks of the armyworm in the grasslands. P = 0.004). The mean estimated yield loss in terms of dry weight An analysis of fecal pellets from an urban environment from the cages with the harvest mouse was 4.68 ± 0.45 g, revealed that seeds, fruit, monocotyledon and dicotyledon leaves, and insects were the primary dietary items of the har- vest mouse; fungi, moss, roots and some other invertebrates were also found to be consumed (Dickman 1986). Although fecal analysis is currently one of the most commonly-used methods for understanding the diet of a mammal, this analysis suffers from some drawbacks (Ruetter et al. 2005). For example, highly digestible food items such as larvae cannot be effectively detected. In fact, the harvest mouse actively may prey on insects including larvae of the armyworm probably to meet its nutritional need for animal protein more often than reported in the published work; this has been suggested through a study of the harvest mouse under captivity with various food items (R. Ishiwaka, unpubl. data). It also supports our hypothesis that several carcasses of the adult armyworm remained in every cage without the harvest mouse Figure 1 Proportions of guineagrass leaves that were classified into when the experiment ceased, meanwhile no carcass was found five categories based on the extent of the leaf area consumed by the in any of the cages with the mice. The lack of feeding signs of armyworm; approximately 100 leaves were randomly sampled from the cages () with and () without the harvest mouse. The vertical bars the harvest mouse detected on guineagrass leaves and signif- indicate standard error of the mean. The frequency distributions of the icant reduction in crop yield loss in the cages with the harvest extent of leaf consumption were significantly different between the mouse suggest that the harvest mouse can function as a presence and absence of the mouse (χ2 analysis, P < 0.0001). natural control agent for the armyworm rather than a pest, at

54 Grassland Science 54 (2008) 52–56 © 2008 Blackwell Publishing Ltd R. Ishiwaka and Y. Masuda Harvest mouse as a control agent least in soling forage crop fields and agricultural grasslands, Donovan BJ (2003) Potential manageable exploitation of social in spite of a general impression of “mice” being a pest. Agri- wasps, Vespula spp. (Hymenoptera: Vespidae), as generalist cultural grasslands are the habitat or feeding places for sev- predators of insect pests. Int J Pest Manage 49: 281–285. eral insectivorous and omnivorous mammal species. Among Ellis JA, Walter AD, Tooker JF, Ginzel MD, Reagel PF, Lacey ES, the omnivorous species, the harvest mouse may prefer insects Bennett AB, Grossman EM, Hanks LM (2005) Conservation on account of its small body size besides food items such as biological control in urban landscapes: manipulating herbaceous plant seeds. parasitoids of bagworm (Lepidoptera: Psychidae) with Cotesia kariyai Watanabe (Hymenoptera: Braconidae) is a flowering forbs. Biol Cont 34: 99–107. specialist parasitoid of the armyworm larvae and thus well Fowler AC, Knight RL, George TL, McEwen LC (1991) Effects of avian predation on grasshopper populations in North Dakota known as a major control agent of this pest insect. In a tritrophic grasslands. Ecology 72: 1775–1781. system consisting of corn plants, the armyworm and C. kariyai, Harris S, Trout RC (1991) Micromys. In: The Handbook of the infested corn plants attracted C. kariyai with herbivore- British Mammals (eds Corbet GB, Harris S). Blackwell induced synomone only when the inflicting larvae were in the Scientific, Oxford, 223–239. early instars (Takabayashi et al. 1995; Hou et al. 2005). The Hirai K, Miyahara Y, Sato M, Fujimura T, Yoshida A (1985) parasitization of young larvae resulted in a decrease in the Outbreaks of the armyworm, Pseudaletia separata Walker damage caused by them, while the parasitization of old larvae (Lepidoptera: Noctuidae) in northern Japan in the mid-July of did not affect the amount of damage caused. It appears that 1984, with analysis of weather maps involved in the ’ corn plants attract C. kariyai only when the recruitment is displacement. Jap J Appl Zool 29: 250–253. adaptive for the plants. In contrast, we observed that, while Hooks CRR, Pandey RR, Johnson MW (2003) Impact of avian under captivity, the harvest mouse preyed on the armyworm and arthropod predation on lepidopteran caterpillar densities larvae without any infested plants; that is, without any and plant productivity in an ephemeral agroecosystem. herbivore-induced synomone (R. Ishiwaka, unpubl. data). Ecol Entomol 28: 522–532. 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